Viability Costs of Reproduction and Behavioral Compensation in Western Mosquitofish (Gambusia affinis)

Belk MC (2014) Viability Costs of Reproduction and Behavioral Compensation in Western Mosquitofish (Gambusia affinis). PLoS ONE 9(11): e110524. doi:10.1371/journal.pone.0110524 Viability Costs of Reproduction and Behavioral Compensation in Western Mosquitofish (Gambusia affinis ) Clinton T. Laidlaw 0 1 Jacob M. Condon 0 1 Mark C. Belk 0 1 Francois Criscuolo, CNRS, France 0 Funding: Funding was provided by The Department of Biology and the Honors Department at Brigham Young University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript 1 Department of Biology, Brigham Young University , Provo, Utah , United States of America The cost of reproduction hypothesis suggests that current reproduction has inherent tradeoffs with future reproduction. These tradeoffs can be both in the form of energy allocated to current offspring as opposed to somatic maintenance and future reproduction (allocation costs), or as an increase in mortality as a result of morphological or physiological changes related to reproduction (viability costs). Individuals may be able to decrease viability costs by altering behavior. Female western mosquitofish, Gambusia affinis experience a reduction in swimming ability as a consequence of pregnancy. We test for a viability cost of reproduction, and for behavioral compensation in pregnant female G. affinis by measuring survival of females in early and later stages of pregnancy when exposed to predation. Late-stage pregnant females experience a 70% greater probability of mortality compared to early-stage pregnant females. The presence of a refuge roughly doubled the odds of survival of both early and late-stage pregnant females. However, there was no interaction between refuge availability and stage of pregnancy. These data do not provide evidence for behavioral compensation by female G. affinis for elevated viability costs incurred during later stages of pregnancy. Behavioral compensation may be constrained by other aspects of the cost of reproduction. - Organisms incur costs to future reproduction as a consequence of current reproduction. The relative amount of energy and time that an organism invests in current reproduction is reflected as a cost to the potential for future reproduction (i.e., cost of reproduction hypothesis; [1], [2]. Costs to future reproduction can be categorized as allocation costs or viability costs. Allocation costs arise because resources allocated to current reproduction cannot be used for future reproduction [1]. Viability costs arise from physiological or morphological changes that result from current reproduction that lead to increased mortality rates compared to non-reproductive individuals [3] Viability costs can result from decreased physiological performance as a consequence of depletion of energy stores (i.e., physiological cost hypothesis; [4], [5]), or from additional morphological changes associated with producing and carrying eggs or developing embryos that produce a decrease in the motility of individuals or their ability to avoid predation (i.e., physical burden hypothesis; [6]; [7]). Some of the most apparent and well-studied consequences of reproduction are those associated with reduced mobility and escape velocity in pregnant or gravid females. Such reduction in mobility has been observed across many taxa; for example, in butterflies [8], fish [7], [9], [10], lizards [11], [12], snakes [5], birds [13], [14], and dolphins [15]. Although declines in performance arising from the physical burden of reproduction have been well documented, few studies have quantified actual cost to survival. In fishes swimming performance is a major determinant of survival probability [16]. Swimming ability (i.e., steady or unsteady swimming measures) is strongly related to body form [1619]. Livebearing fishes show a change in body form and increased overall mass in the latter stages of pregnancy. For example, in the livebearing fish Brachyrhaphis rhabdophora, females exhibit increased abdominal distension as pregnancy progresses [20], [21]. Pregnancy-related reduction in escape velocity has been observed in western mosquitofish (Gambusia affinis) [22], [23] and these studies have suggested that females experience a viability cost of reproduction as a consequence of the physical burden of livebearing. The argument is that changes in shape lead to reduced swimming ability which leads to increased mortality of pregnant females. However, the magnitude of this viability cost of reproduction associated with pregnancy or gravidity has rarely been quantified in vertebrates [24]. In response to an increase in predation risk, many organisms modify their behavior to reduce the probability of mortality. The threat-sensitivity hypothesis predicts that prey increase antipredator behavior as risk of mortality increases [25], [26]. Many species avoid risky habitats, increase refuge use, or stay closer to refuge habitat when predators are near [10], [2729]. Behavioral change in the frequency of use of refuges during times of increased predation risk should result in increased survival probabilities [30]. Organisms that effectively reduce viability costs can potentially gain higher lifetime fecundity and increase overall fitness. Selection should favor behavioral compensation to reduce viability costs of reproduction as long as the benefit to fitness (such as additional reproductive opportunities) outweighs the cost (reduced opportunity for foraging or other activities, i.e., [31]). Livebearing fishes exhibit antipredator behaviors including use of refuge habitats [32], [33]. However, how refuge availability influences viability costs of reproduction is not well known. Previous work on livebearing fishes suggests that reduced locomotory performance associated with pregnancy is likely to result in increased mortality in pregnant females especially at later stages of pregnancy [18], [3436], and that pregnant females should compensate for this increased probability of mortality by increasing the use of refuge habitats at later stages of pregnancy [27], [37]. However, we found no published studies that quantified viability costs of reproduction and refuge effects as a consequence of pregnancy. In this study, we test for viability costs of reproduction in female western mosquitofish (Gambusia affinis) by comparing mortality rates of early and late-term pregnant females to see if risk of predation increases with increasing volume during pregnancy. Additionally, we test whether pregnant females will use refuges with increased frequency as a means of behaviorally compensating for reduced escape velocity and increased susceptibility to predation. All animal work was done with the approval and supervision of the Institutional Animal Care and Use Committee at Brigham Young University. No regulations were broken. Permits were obtained from the Utah Division of Wildlife Resources f (...truncated)